Persistent, Long-term Cerebral White Matter Changes after Sports-Related Repetitive Head Impacts

Introduction Repetitive head impacts (RHI) sustained in contact sports are thought to be necessary for the long-term development of chronic traumatic encephalopathy (CTE). Our objectives were to: 1) characterize the magnitude and persistence of RHI-induced white matter (WM) changes; 2) determine their relationship to kinematic measures of RHI; and 3) explore their clinical relevance. Methods Prospective, observational study of 10 Division III college football players and 5 non-athlete controls during the 2011-12 season. All subjects underwent diffusion tensor imaging (DTI), physiologic, cognitive, and balance testing at pre-season (Time 1), post-season (Time 2), and after 6-months of no-contact rest (Time 3). Head impact measures were recorded using helmet-mounted accelerometers. The percentage of whole-brain WM voxels with significant changes in fractional anisotropy (FA) and mean diffusivity (MD) from Time 1 to 2, and Time 1 to 3 was determined for each subject and correlated to head impacts and clinical measures. Results Total head impacts for the season ranged from 431–1,850. No athlete suffered a clinically evident concussion. Compared to controls, athletes experienced greater changes in FA and MD from Time 1 to 2 as well as Time 1 to 3; most differences at Time 2 persisted to Time 3. Among athletes, the percentage of voxels with decreased FA from Time 1 to 2 was positively correlated with several helmet impact measures. The persistence of WM changes from Time 1 to 3 was also associated with changes in serum ApoA1 and S100B autoantibodies. WM changes were not consistently associated with cognition or balance. Conclusions A single football season of RHIs without clinically-evident concussion resulted in WM changes that correlated with multiple helmet impact measures and persisted following 6 months of no-contact rest. This lack of WM recovery could potentially contribute to cumulative WM changes with subsequent RHI exposures.

[1]  Andrew R. Mayer,et al.  Functional magnetic resonance imaging of mild traumatic brain injury , 2015, Neuroscience and Biobehavioral Reviews.

[2]  J. Corrigan,et al.  Initial Reliability and Validity of the Ohio State University TBI Identification Method , 2007, The Journal of head trauma rehabilitation.

[3]  J. Povlishock,et al.  Intensity- and interval-specific repetitive traumatic brain injury can evoke both axonal and microvascular damage. , 2012, Journal of neurotrauma.

[4]  E. Ewert Assessment and Management of Sport-related Concussions in United States High Schools , 2012 .

[5]  J. Gilger,et al.  Biomechanical correlates of symptomatic and asymptomatic neurophysiological impairment in high school football. , 2012, Journal of biomechanics.

[6]  T. Talavage,et al.  Functionally-detected cognitive impairment in high school football players without clinically-diagnosed concussion. , 2014, Journal of neurotrauma.

[7]  A. McKee,et al.  Chronic Traumatic Encephalopathy in Athletes: Progressive Tauopathy After Repetitive Head Injury , 2009, Journal of neuropathology and experimental neurology.

[8]  Chengjie Xiong,et al.  Multiplexed Immunoassay Panel Identifies Novel CSF Biomarkers for Alzheimer's Disease Diagnosis and Prognosis , 2011, PloS one.

[9]  Peter Cameron,et al.  The Evidence for Chronic Traumatic Encephalopathy in Boxing , 2007, Sports medicine.

[10]  J J Crisco,et al.  Solitary sclerosis: Progressive myelopathy from solitary demyelinating lesion , 2012, Neurology.

[11]  Kevin M. Guskiewicz,et al.  Assessment of Mild Head Injury Using Measures of Balance and Cognition: A Case Study , 1997 .

[12]  Jason P Mihalik,et al.  MEASUREMENT OF HEAD IMPACTS IN COLLEGIATE FOOTBALL PLAYERS: AN INVESTIGATION OF POSITIONAL AND EVENT‐TYPE DIFFERENCES , 2007, Neurosurgery.

[13]  Tong Zhu,et al.  Subject-specific changes in brain white matter on diffusion tensor imaging after sports-related concussion. , 2012, Magnetic resonance imaging.

[14]  J. Sosnoff,et al.  Biomechanical properties of concussions in high school football. , 2010, Medicine and science in sports and exercise.

[15]  G. Siest,et al.  Decreased high-density lipoprotein cholesterol and serum apolipoprotein AI concentrations are highly correlated with the severity of Alzheimer’s disease☆ , 2000, Neurobiology of Aging.

[16]  Paul McCrory,et al.  Validity and reliability of the Nintendo Wii Balance Board for assessment of standing balance. , 2010, Gait & posture.

[17]  A. Uluğ,et al.  Diffusion anisotropy changes in the brains of professional boxers. , 2006, AJNR. American journal of neuroradiology.

[18]  Grant L Iverson,et al.  On-Field Predictors of Neuropsychological and Symptom Deficit Following Sports-related Concussion , 2003, Clinical journal of sport medicine : official journal of the Canadian Academy of Sport Medicine.

[19]  Erik D Power,et al.  Forensic injury biomechanics. , 2007, Annual review of biomedical engineering.

[20]  A. McKee,et al.  Long‐term Consequences of Repetitive Brain Trauma: Chronic Traumatic Encephalopathy , 2011, PM & R : the journal of injury, function, and rehabilitation.

[21]  R. Wennberg,et al.  Absence of chronic traumatic encephalopathy in retired football players with multiple concussions and neurological symptomatology , 2013, Front. Hum. Neurosci..

[22]  K. Blennow,et al.  Neurochemical aftermath of amateur boxing , 2006, Archives of neurology.

[23]  A. J. McLean,et al.  Stalning af amyloid percursor protein to study axonal damage in mild head Injury , 1994, The Lancet.

[24]  D. T. Vernier,et al.  Restriction isotyping of human apolipoprotein E by gene amplification and cleavage with HhaI. , 1990, Journal of lipid research.

[25]  A. Buki,et al.  All roads lead to disconnection? – Traumatic axonal injury revisited , 2006, Acta Neurochirurgica.

[26]  Maximilian Reiser,et al.  White matter integrity in the brains of professional soccer players without a symptomatic concussion. , 2012, JAMA.

[27]  A J McLean,et al.  Topography of axonal injury as defined by amyloid precursor protein and the sector scoring method in mild and severe closed head injury. , 1995, Journal of neurotrauma.

[28]  J. Saczynski,et al.  The relation between apolipoprotein A-I and dementia: the Honolulu-Asia aging study. , 2007, American journal of epidemiology.

[29]  A. McKee,et al.  The spectrum of disease in chronic traumatic encephalopathy. , 2013, Brain : a journal of neurology.

[30]  J. Langlois,et al.  The Epidemiology and Impact of Traumatic Brain Injury: A Brief Overview , 2006, The Journal of head trauma rehabilitation.

[31]  Sarah K Fields,et al.  Epidemiology of Concussions Among United States High School Athletes in 20 Sports , 2012, The American journal of sports medicine.

[32]  Ann C. McKee,et al.  Chronic traumatic encephalopathy: neurodegeneration following repetitive concussive and subconcussive brain trauma , 2012, Brain Imaging and Behavior.

[33]  James C. Ford,et al.  Effect of head impacts on diffusivity measures in a cohort of collegiate contact sport athletes , 2014, Neurology.

[34]  Joseph T. Gwin,et al.  HEAD IMPACT SEVERITY MEASURES FOR EVALUATING MILD TRAUMATIC BRAIN INJURY RISK EXPOSURE , 2008, Neurosurgery.

[35]  D. Norris,et al.  Physical activity is related to the structural integrity of cerebral white matter , 2013, Neurology.

[36]  J. Bazarian,et al.  Bench to bedside: evidence for brain injury after concussion--looking beyond the computed tomography scan. , 2006, Academic emergency medicine : official journal of the Society for Academic Emergency Medicine.

[37]  J. Crisco,et al.  Frequency and location of head impact exposures in individual collegiate football players. , 2010, Journal of athletic training.

[38]  M. Kamboh,et al.  Emerging Histomorphologic Phenotypes of Chronic Traumatic Encephalopathy in American Athletes , 2011, Neurosurgery.

[39]  J. Zhong,et al.  Consequences of Repeated Blood-Brain Barrier Disruption in Football Players , 2013, PloS one.

[40]  G. Will “Punch Drunk” , 1939 .

[41]  Jay Smith,et al.  Intrarater and Interrater Reliability of the Balance Error Scoring System (BESS) , 2009, PM & R : the journal of injury, function, and rehabilitation.

[42]  A J McLean,et al.  Staining of amyloid precursor protein to study axonal damage in mild head injury. , 1994, Lancet.

[43]  A. Fagan,et al.  Multimodal techniques for diagnosis and prognosis of Alzheimer's disease , 2009, Nature.

[44]  Sylvain Bouix,et al.  Scholarship@Western Scholarship@Western , 2022 .